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Differential Expression of Rice Lambda Class GST Gene Family Members During Plant Growth, Development, and in Response to Stress Conditions

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Abstract

Glutathione S-transferases (GSTs; EC 2.5.1.18) are members of an isozyme family and catalyze the conjugation of the reduced tripeptide glutathione to a variety of hydrophobic and electrophilic substrates. Though members of different classes of the GST superfamily have been identified and characterized from many plant species including rice, no detailed information is available for the Lambda class gene family in rice. In this study, a genome-wide analysis was carried out to investigate expression patterns of three Lambda class GST members of rice including OsGSTL1, OsGSTL2 and OsGSTL3 in seedlings, at different growth and developmental stages as well as in response to various biotic and abiotic stresses. Expression analysis using microarray datasets and quantitative real-time reverse transcriptase polymerase chain reaction suggests that this gene family express differentially in various tissues, in response to hormones and during different biotic and abiotic stresses including heavy metals, cold, drought and salt stress. Massively Parallel Signature Sequencing (MPSS) analysis also showed differential expression of OsGSTLs during plant growth and development and under different stresses. Out of three members, maximum expression of OsGSTL2 was observed for the MPSS libraries in comparison to other members. We conclude that members of rice Lambda class GST family play an important role in plant growth and development and in combating different biotic and abiotic stresses.

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References

  • Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J, Corcoran K (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18:630–634

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D, Kumar S, Rai A, Pandey A, Nigam D (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74:688–702

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarty D, Trivedi PK, Shri M, Misra P, Asif MH, Dubey S, Kumar S, Rai A, Tiwari M, Shukla D, Pandey A, Nigam D, Tripathi RD, Tuli R (2010) Differential transcriptional expression following thidiazuron-induced callus differentiation developmental shifts in rice. Plant Biol 12:46–59

    Article  PubMed  CAS  Google Scholar 

  • Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351

    Article  PubMed  CAS  Google Scholar 

  • Choi JH, Jung HY, Kim HS, Cho HG (2000) PhyloDraw: a phylogenetic tree drawing system. Bioinformatics 16:1056–1058

    Article  PubMed  CAS  Google Scholar 

  • Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280

    Article  PubMed  CAS  Google Scholar 

  • Dean JD, Goodwin PH, Hsiang T (2005) Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56:1525–1533

    Article  PubMed  CAS  Google Scholar 

  • Diao G, Wang Y, Wang C, Yang C (2011) Cloning and functional characterization of a novel glutathione S-transferase gene from Limonium bicolor. Plant Mol Biol Report 29:77–87

    Article  CAS  Google Scholar 

  • Dirr H, Reinemer P, Huber R (1994) X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function. Eur J Biochem 220:645–661

    Article  PubMed  CAS  Google Scholar 

  • Dixit P, Mukherjee PK, Ramachandran V, Eapen S (2011) Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6:e16360

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxifucation systems in plants. Curr Opin Plant Biol 1:258–266

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Sellars JD, Edwards R (2011a) The Arabidopsis phi class glutathione transferase AtGSTF2: binding and regulation by biologically active heterocyclic ligands. Biochem J 438:63–70

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Steel PG, Edwards R (2011b) Roles for glutathione transferases in antioxidant recycling. Plant Signal Behav 8:1223–1227

    Article  Google Scholar 

  • Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag SK, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genomics 11:648

    Article  PubMed  Google Scholar 

  • Eaton DL, Bammler TK (1999) Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol Sci 49:156–164

    Article  PubMed  CAS  Google Scholar 

  • Edwards R, Del Buono D, Fordham M, Skipsey M, Brazier M, Dixon DP, Cummings I (2005) Differential induction of glutathione transferases and glucosyltransferases in wheat, maize and Arabidopsis thaliana by herbicide safeners. Z Naturforsch C 60:307–316

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6.. Department of Genome Sciences, University of Washington, Seattle, Distributed by the author

    Google Scholar 

  • Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Hossain MZ (2003) Modulation of pumpkin glutathione S-transferases by aldehydes and related compounds. Plant Cell Physiol 44:481–490

    Article  PubMed  CAS  Google Scholar 

  • Gautam N, Verma PK, Verma S, Tripathi RD, Trivedi PK, Adhikari B, Chakrabarty D (2012) Genome-wide identification of rice class I metallothionein gene: tissue expression patterns and induction in response to heavy metal stress. Funct Integr Genomics. doi:10.1007/s10142-012-0297-9

  • George S, Venkataraman G, Parida A (2009) A chloroplast-localized and auxin-induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318

    Article  PubMed  Google Scholar 

  • Ghelfi A, Gaziola SA, Cia MC, Chabregas SM, Falco MC, Kusar-Falcao PR, Azevedo RA (2011) Cloning, expression, molecular modelling and docking analysis of glutathione transferase from Saccharum officinarum. Ann Appl Biol 159:267–280

    Article  CAS  Google Scholar 

  • Gong H, Jiao Y, Hu WW, Pua EC (2005) Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro. Plant Mol Biol 57:53–66

    Article  PubMed  CAS  Google Scholar 

  • Hernandez I, Alegre L, Bosch SM (2004) Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol 24:1303–1311

    Article  PubMed  CAS  Google Scholar 

  • Hershey HP, Stoner TD (1991) Isolation and characterization of cDNA clones for RNA species induced by substituted benzenesulfonamides in corn. Plant Mol Biol 17:679–690

    Article  PubMed  CAS  Google Scholar 

  • Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H (2007) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83

    Article  PubMed  Google Scholar 

  • Hu T, Qv X, Xiao G, Huang X (2009) Enhanced tolerance to herbicide of rice plants by over-expression of a glutathione S-transferase. Mol Breeding 24:409–418

    Article  CAS  Google Scholar 

  • Hu TZ, He S, Huang XY, Deng L, Wang GX (2011a) Cloning, molecular characterization and heterologous expression of a glutathione S-transferase gene in rice. Bioorg Khim 37:386–392

    PubMed  CAS  Google Scholar 

  • Hu T, He S, Yang G, Zeng H, Wang G, Chen Z, Huang X (2011b) Isolation and characterization of a rice glutathione S-transferase gene promoter regulated by herbicides and hormones. Plant Cell Rep 30:539–549

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genomics 11:73

    Article  PubMed  Google Scholar 

  • Ji W, Zhu Y, Li Y, Yang L, Zhao X, Cai H, Bai X (2010) Over-expression of a glutathione S-transferase gene, GsGST, from wild soybean (Glycine soja) enhances drought and salt tolerance in transgenic tobacco. Biotechnol Lett 32:1173–1179

    Article  PubMed  CAS  Google Scholar 

  • Kim SI, Andaya VC, Tai TH (2011) Cold sensitivity in rice (Oryza sativa L.) is strongly correlated with a naturally occurring I99V mutation in the multifunctional glutathione transferase isoenzyme GSTZ2. Biochem J 435:373–380

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Trivedi PK (2011) Differential expression and alternative splicing of rice sulphate transporter family members regulate sulphur status during plant growth, development and stress conditions. Funct Integr Genomics 11:259–273

    Article  PubMed  CAS  Google Scholar 

  • Kunieda T, Fujiwara T, Amano T, Shioi Y (2005) Molecular cloning and characterization of a senescence-induced tau-class glutathione S-transferase from barley leaves. Plant Cell Physiol 46:1540–1548

    Article  PubMed  CAS  Google Scholar 

  • Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wang WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98:31–36

    Article  PubMed  CAS  Google Scholar 

  • Martret BL, Poage M, Shiel K, Nugent GD, Dix PJ (2011) Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J 9:661–673

    Article  PubMed  Google Scholar 

  • McGonigle B, Keeler SJ, Lau SM, Koeppe MK, O’Keefe DP (2000) A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol 124:1105–1120

    Article  PubMed  CAS  Google Scholar 

  • Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakrabarty D, Singh PK, Trivedi PK, Nath P, Tuli R (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268

    Article  PubMed  CAS  Google Scholar 

  • Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitam Horm 72:155–202

    Article  PubMed  CAS  Google Scholar 

  • Nakano M, Nobuta K, Vemaraju K, Tej SS, Skogen JW, Meyers BC (2006) Plant MPSS databases: signature-based transcriptional resources for analyses of mRNA and small RNA. Nucleic Acids Res 34:D731–D735

    Article  PubMed  CAS  Google Scholar 

  • Norton GJ, Lou-Hing DE, Meharg AA, Price AH (2008) Rice–arsenate interactions in hydroponics: whole genome transcriptional analysis. J Exp Bot 59:2267–2276

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  PubMed  CAS  Google Scholar 

  • Pandey A, Misra P, Chandrashekar K, Trivedi PK (2012) Development and optimization of AtMYB12 expressing transgenic tobacco callus culture for large scale production of rutin with biopesticidal potential. Plant Cell Rep 31:1867–1876

    Article  PubMed  CAS  Google Scholar 

  • Qi YC, Liu WQ, Qiu LY, Zhang SM, Ma L, Zhang H (2010) Overexpression of glutathione S-transferase gene increases salt tolerance of Arabidopsis. Russ J Plant 57:233–240

    Article  CAS  Google Scholar 

  • Rai A, Tripathi P, Dwivedi S, Dubey S, Shri M, Kumar S, Tripathi PK, Dave R, Kumar A, Singh R, Adhikari B, Bag M, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2011) Arsenic tolerances in rice (Oryza sativa) have a predominant role in transcriptional regulation of a set of genes including sulphur assimilation pathway and antioxidant system. Chemosphere 82:986–995

    Article  PubMed  CAS  Google Scholar 

  • Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK (2010) In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res 17:139–153

    Article  PubMed  CAS  Google Scholar 

  • Ribot C, Hirsch J, Balzergue S, Tharreau D, Nottéghem JL, Lebrun MH, Morel JB (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea. J Plant Physiol 165:114–124

    Article  PubMed  CAS  Google Scholar 

  • Roxas VP, Smith RK Jr, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    Article  PubMed  CAS  Google Scholar 

  • Rushmore TH, Pickett CB (1993) Glutathione S-transferases, structure, regulation, and therapeutic implications. J Biol Chem 268:11475–11478

    PubMed  CAS  Google Scholar 

  • Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Harvey Millar A, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68

    Article  PubMed  CAS  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110

    Article  PubMed  CAS  Google Scholar 

  • Soranzo N, Sari Gorla M, Mizzi L, De Toma G, Frova C (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271:511–521

    Article  PubMed  CAS  Google Scholar 

  • Swarbrick PJ, Huang K, Liu G, Slate J, Press MC, Scholes JD (2008) Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. New Phytol 179:515–529

    Article  PubMed  CAS  Google Scholar 

  • Takesawa T, Ito M, Kanzaki H, Kameya N, Nakamura I (2002) Over-expression of ζ glutathione S-transferase in transgenic rice enhances germination and growth at low temperature. Mol Breeding 9:93–101

    Article  CAS  Google Scholar 

  • Theodoulou F, Clark IM, He XL, Pallett KE, Cole DJ, Hallahan DL (2003) Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Manag Sci 59:202–214

    Article  PubMed  CAS  Google Scholar 

  • Tsuchiya T, Takesawa T, Kanzaki H, Nakamura I (2004) Genomic structure and differential expression of two tandem-arranged GSTZ genes in rice. Gene 335:141–149

    Article  PubMed  CAS  Google Scholar 

  • Tuli R, Chakrabarty D, Trivedi PK, Tripathi RD (2010) Recent advances in arsenic accumulation and metabolism in rice. Mol Breeding 26:307–323

    Article  CAS  Google Scholar 

  • Urbanek H, Majorowicz H, Zalewski M, Saniewski M (2005) Induction of glutathione S-transferase and glutathione by toxic compounds and elicitors in reed canary grass. Biotechnol Lett 27:911–914

    Article  PubMed  CAS  Google Scholar 

  • Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532

    Article  PubMed  CAS  Google Scholar 

  • Zhao FY, Liu W, Zhang SY (2009) Different responses of plant growth and antioxidant system to the combination of cadmium and heat stress in transgenic and non-transgenic rice. J Integr Plant Biol 51:942–950

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Goldsbrough PB (1993) An Arabidopsis gene with homology to glutathione S-transferase is regulated by ethylene. Plant Mol Biol 22:517–523

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by research grants from the Council of Scientific and Industrial Research, New Delhi, as Network Project and Department of Science and Technology, New Delhi. SK acknowledges the Council of Scientific and Industrial Research Govt. of India for Senior Research Fellowship.

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Correspondence to Prabodh Kumar Trivedi.

Electronic Supplementary Materials

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Supplementary Table S1

Details of rice microarray experiments from GEO database used in the study (DOC 71 kb)

Supplementary Table S2

List of oligonucleotides used for the analysis (DOC 30 kb)

Supplementary Table S3

MPSS library information used for the OsGSTLs analysis (DOC 56 kb)

Supplementary Table S4

List of all AtGSTs and OsGSTs, In2-1 proteins considered for the phylogenetic analysis (DOC 86 kb)

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Kumar, S., Asif, M.H., Chakrabarty, D. et al. Differential Expression of Rice Lambda Class GST Gene Family Members During Plant Growth, Development, and in Response to Stress Conditions. Plant Mol Biol Rep 31, 569–580 (2013). https://doi.org/10.1007/s11105-012-0524-5

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